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Study areaThe study area is located in Lintong District, Xi’an City, Shaanxi Province, China (34° 21′ 59.94″, 109° 12′ 51.012″) (Meteorologists, 2020b). The study area is located in northwestern China (Fig. 1), which is a Warm temperate semi-humid continental climate with distinct cold, warm, dry and wet seasons. Winter is cold, windy, foggy, and with little rain or snow. Spring is warm, dry, windy, and variable. The summer is hot and rainy, with prominent droughts and thunderstorms, and high wind. Autumn is cool, the temperature drops rapidly and autumn showers are obvious. The annual average temperature is 13.0–13.7 °C, the coldest January average temperature is −1.2–0 °C, the hottest July average temperature is 26.3–26.6 °C, the annual extreme minimum temperature is −21.2 °C, Lantian December 28, 1991, the annual extreme maximum temperature is 43.4 °C, Chang’an June 19, 1966. Annual precipitation is 522.4–719.5 mm, increasing from north to south. July and September are the two obvious peak precipitation months. The annual sunshine hours range from 1646.1 to 2114.9 h. The dominant wind direction varies from place to place, with the northeast wind in Xi’an, west wind in Zhouzhi and Huxian, east-northeast wind in Gaoling and Lintong, southeast wind in Chang’an, and northwest wind in Lantian. Meteorological disasters include drought, continuous rain, heavy rain, flooding, urban flooding, hail, gale, dry hot wind, high temperature, lightning, sand and dust, fog, haze, cold wave, and low-temperature freeze.
Figure 1Location of the field of study (The satellite imagery supporting this study was obtained using Baidu Maps (Android version—16.4.0.1195). The URL is (https://map.baidu.com/@14256795.568410998,5210675.606268121,8.67z.).Full size imageWheat (XiNong 805) was planted on September 24, 2019 and matured for harvest on May 28, 2020 (We warrant that we have the right to collect and manage wheat (XiNong 805). In addition, the study is in compliance with relevant institutional, national, and international guidelines.). Among the six strategies in the experiment (Table 1), we focused on strategies 1 and 4, fixed irrigation dates optimization and fixed fertilizer application dates optimization. Based on the custom of the study area, three days of diffuse irrigation were selected for Strategy 1. Three days of fertilization of the urea and three days of irrigation were selected for Strategy 4. The best practice for Strategy 1 was total irrigation of 201 mm for the total season and a total of 7388 kg/ha of wheat was obtained for this simulation, while the best practice for Strategy 4 was total irrigation of 197 mm for the total season and a total fertilizer application of 282 kg/ha for the total season. A total of 7894 kg/ha of wheat was obtained for this simulation.Table 1 Details of the 6 strategies of the experimental setup.Full size tableDSSAT modelDSSAT, one of the most widely used crop growth models, is an integrated computer system developed by the University of Hawaii under the authority of the U.S. Agency for International Development (USAID). It aims to aggregate various crop models and standardize the format of model input and output variables to facilitate the diffusion and application of models7, thereby accelerating the diffusion of agricultural technology and providing decision making and countermeasures for the rational and efficient use of natural resources in developing countries.
The DSSAT 4.5 model integrates all crop models into the simulation pathway-based CSM (Cropping System Model) farming system model, which uses a set of simulated soil moisture, nitrogen, and carbon dynamics codes, while crop growth and development are stimulated through the CERES37,38, CROPGRO39, CROPSIM, and SUBSOR modules. DSSAT is applicable to single sites or same type zones and can be extrapolated to the regional level through Geographic Information System (GIS).DSSAT–CSM simulates the growth process of crops grown on a uniform land area under prescribed or simulated management40, and the changes in soil water, carbon and nitrogen with under tillage systems. The DSSAT model is a decision support system supported by crop simulation models, which, in addition to data support, provides methods for calculating and solving problems, and provides decision-maker with the results of their decisions. It also provides scientific decisions for farmers to provide different cultivation management measures (e.g., proper fertilization and irrigation for crops) in different climatic years.Inputs and outputs of the modelThe DSSAT model has four main user-editable input files and various output files. The input files include crop management7,41, soil, weather, and cultivar parameter files; the output files include three types: (1) output files, (2) seasonal output files, and (3) diagnostic and management files.Crop management data: Crop management data provides basic information about crop growth. Detailed and accurate parameter provision is the basis for improving the accuracy of model simulation. Crop management parameters include crop variety, soil type, meteorological name, previous season crop, sowing period, sowing density, sowing depth, irrigation amount and time, fertilizer application amount and time, the initial condition of the soil, pest management, tillage frequency and method, etc. Some of these parameters are not easily available in field experiments and can be obtained from other test sites or from existing documentation. On the other hand, if there are missing values in the model, it will increase the simulation error of the model (this situation is hard to avoid). Therefore, in this study, the parameters were selected based on the principle of being both detailed and easily available.Soil data Soil data contains various parameters of the soil section plane, including soil color, soil slope, soil capacity, organic carbon, soil nitrogen content, drainage properties, the proportion of clay, particles, and stones in the soil. Similar to the governing documents, the more complete the parameters the smaller the error value of the simulation. The various physical and chemical properties of the soil for this study were obtained from the China Soil Database at the time of the study. The various physical and chemical properties of the soil for this study were obtained from the China Soil Database.Weather data The DSSAT model uses daily weather data as weather input data for the model. The model requires a minimum of four daily weather data in order to accurately simulate the water cycle in soil plants (Fig. 2). These are:(1) daily solar radiation energy (MJM); (2) daily maximum temperature (°C); (3) daily minimum temperature (°C); and (4) daily precipitation (mm). Weather data were obtained from the China Meteorological Administration. Weather data were obtained from the China Meteorological Administration.Figure 2Precipitation and maximum and minimum temperatures during 2019–2020.Full size imageModel calibration Adjusting the cultivar parameter is very important to accurately simulate the local growing environment. In this experiment, we collected field data for 2019 and 2020, and adjusted the parameters in the cultivar parameter files by trial-and-error method to make the simulation process more closely match the actual local crop growth process.Multi-objective optimization algorithmMulti-objective optimization techniques have been successfully applied in many real-world problems. In general42,43,44, MOPs produce a set of optimal solutions that together represent a trade-off between conflicting objectives, and such solutions are called Pareto optimal solutions (PS). These PS cannot make any solution better without compromising the other solutions. Therefore, when solving multi-objective problems, more PS are needed to find. Some MOPs aim to find all PS or at least a representative subset of them.A multi-objective optimization problem can be stated as follows:$$mathrm{min }Fleft(xright)={({f}_{1}left(xright),dots ,{f}_{k}(x))}^{T}$$
(1)
$$mathrm{subject;to};xin Omega$$
(2)
where (Omega) is the decision space,(F:Omega to {R}^{k}) consists of (k) real-value objective functions and ({R}^{k}) is called the objective space. The attainable objective set is defined as the set ({F(x)in Omega }).NSGA-II optimizerWe use non-dominated sorting genetic algorithm (NSGA-II) for Multiobjective optimization in R language. The NSGA-II algorithm is a classical multi-objective evolutionary algorithm with remarkable results in solving 2-objective and 3-objective problems45. It maintains the convergence speed and diversity of solutions by fast non-dominated sorting and crowding distance, selects the next population by elite selection strategy.Objective functionThe multi-objective optimization problem varies one or more variables to maximize or minimize two or more objective problems. In the case of crop production, where decision-makers change irrigation and fertilizer application to maximize benefits, this study focuses on when to apply irrigation or fertilizer on the field and how much irrigation or nitrogen fertilizer to apply.There are many crop models available that can be used as optimization objective functions, and DSSAT is definitely the best choice because it is easy to use and well-proven36. The user runs the model by entering defined soil, weather, variety, and crop management files, which are fed into the core of the model, the Crop Simulation Model (CSM). The model simulates the growth, development, and yield of crops grown on a uniform land area under management, as well as changes in soil water, carbon, and nitrogen over time under cropping systems. The CSM itself is a highly modular model system consisting of a number of sub-modules. Researchers have validated the output of these sub-modules as a whole under various crops, climate, and soil conditions.Using DSSAT, it is easy to design a set of objective functions and optimize them, as in our case.$$mathrm{Max}:Y=mathrm{DSSAT}left.left( {i}_{a0},dots ,{i}_{mathrm{aj}},{f}_{mathrm{a}0},dots ,{f}_{mathrm{ad}},{D}_{i}right.right)$$
(3)
$$mathrm{Min}:I=sum_{n=0}^{j}{i}_{an}$$
(4)
$$mathrm{Min}:F=sum_{m=0}^{d}{f}_{am}$$
(5)
where (Y) is yield,(I) is the total amount of irrigation, (F) is the total amount of nitrogen application, ({i}_{an}) is the amount of irrigation at one time, ({f}_{am}) is the amount of nitrogen applied at one time, (j) is a number of applications of irrigation, and (d) is a number of nitrogen applications. ({D}_{i}) is a random date combination of irrigation time and fertilizer application time.All other variables (e.g., climate, soil, location, crop variety) are kept constant during the optimization process. The irrigation unit is mm and the nitrogen application unit is kg/ha, the irrigation and nitrogen application amounts are positive integers by default (integer arithmetic reduces the program running time).Data-driven evolutionary algorithmsIn general, the key to DDEAs is to reduce the required FEs and assist evolution through data. The data is generally utilized through surrogate model. The use of suitable surrogate model can be used in place of real FEs46. Thus, DDEAs have more advantages over EAs in solving expensive problems.In terms of algorithmic framework, DDEAs contain two parts: surrogate model management (SMM) and evolutionary optimization part (EOP)47,48. The SMM part is used in order to obtain better approximations, while EOPs will use surrogate models in EAs to assist evolution. DDEAs can be divided into two types: online DDEAs and offline DDEAs23. Online DDEAs can be evaluated by real FEs with more new data. This new information can provide SMM with more information and construct a more accurate surrogate model49. Since DSSAT can obtain new data through FEs during the EOP process, the method used in this paper is online DDEAs. In contrast, offline DDEAs can only drive evolution through historical data.Radial Basis Function (RBF) network is a single hidden layer feedforward neural network that uses a radial basis function as the activation function for the hidden layer neurons, while the output layer is a linear combination of the outputs of the hidden layer neurons. RBF was used to approximate each objective function. According to the investigation of multi-objective optimization problems with high computational cost, radial basis functions are often used as the surrogate model, mainly because RBF networks can approximate arbitrary nonlinear functions with arbitrary accuracy and have global approximation capability, which fundamentally solves the local optimum problem of BP networks, and the topology is compact, the structural parameters can be learned separately, and the convergence speed is fast.In this paper, a new data-driven approach is proposed and place it in the lower-level optimization of the framework. RBF is utilized as the surrogate model and NSGA-II as the optimizer. Details are described in Algorithm 1.Data-driven method details
In step 1, the initial parent population is generated by randomly selecting points and the size is (N). In step 2, we run DSSAT (N) times to determine the objective function values of the (N) initial population solutions. Next, the algorithm then loops through the generations. At the beginning of each loop, surrogate models, which one objective train one surrogate and denoted by ({s}_{t}^{left({f}_{1}right)}) , were trained by the already obtained objective function values (step 3.1). The trial offspring ({P}_{i}^{^{prime}}left(tright)={ {x}_{1}^{^{prime}}left(tright),dots ,{x}_{u}^{^{prime}}left(tright)}) are generated by SBX and PM (step 3.2), then the trained surrogate model is used to predict the objective function values of trial offspring (step 3.3). The predicted objective function values are sorting by Pareto non-dominated and crowding distance (step 3.4), then (r) offspring (Q_{i} left( t right) = left{ {x^{primeprime}_{1} left( t right), ldots ,x^{primeprime}_{r} left( t right)} right}) are selected from the trial offspring (step 3.5).The offspring are evaluated by the DSSAT (step 3.6), and after combining the parent population and offspring population (step 3.7), the new parent population are selected by Pareto non-dominated and crowding distance sorting (step 3.8).Maximum extension distanceMED guides a small number of individuals to approximate the entire PF. MED is defined as follow:$$mathrm{MED}left({P}_{t}^{left(qright)}right)=mathrm{ND}left({P}_{t}^{left(qright)}right)times mathrm{TD}left({P}_{t}^{left(qright)}right)$$
(6)
where$$mathrm{ND}left({P}_{t}^{left(qright)}right)=underset{z,qne z}{mathrm{min}}sum_{m=1}^{M}left|{f}_{m}^{left(qright)}-{f}_{m}^{left(zright)}right|$$$$mathrm{TD}left({P}_{t}^{left(qright)}right)=sum_{z=1}^{P}sum_{m=1}^{M}left|{f}_{m}^{left(qright)}-{f}_{m}^{left(zright)}right|$$({P}_{t}^{left(qright)}) is the qth individual in population Pt at the tth generation. (mathrm{ND}left({P}_{t}^{left(qright)}right)) calculates the minimum distance between ({P}_{t}^{left(qright)}) and ({P}_{t}^{left(zright)}). The larger (mathrm{ND}left({P}_{t}^{left(qright)}right)) value means a better individual diversity. (mathrm{TD}left({P}_{t}^{left(qright)}right)) calculates the summation of distance between ({P}_{t}^{left(qright)}) and ({P}_{t}^{left(zright)}). The larger (mathrm{TD}left({P}_{t}^{left(qright)}right)) value means that the solution ({P}_{t}^{left(qright)}) has moved away from other individuals. A larger MED value means that an individual extends the overall boundary and an individual acquires better diversity.Modeling processTo maximize crop yield and optimize the use efficiency of water and fertilizer in a given environment, BSBOP framework is proposed. Crop growth is simulated by DSSAT, the data-driven approach reduces the runtime of the overall framework while finding optimal management strategies. The overall framework includes four main parts: upper-level screening, upper-level optimization, lower-level optimization and lower-level screening (Fig. 3).Figure 3Proposed integrated bi-level screening, bi-level optimization and DSSAT framework.Full size imageUpper-level screening The weather file in DSSAT was loaded by R language. The data are pre-processed with precipitation and solar radiation information to narrow down the date range for irrigation and fertilizer application. In other words, the date ranges for selecting irrigation and fertilization are restricted by the ULS.Upper-level optimization Generating random combinations of dates by the Latin hypercube sampling method (LHS). The upper-level screening starts with referencing the two variables (number of irrigation and nutrient application events). LHS uses these variables to generate a series of uniformly distributed random day combinations. For example, date combinations generated by the LHS could be May 15, July 18 and August 1 for irrigation and May 30, June 30 and July 18 for nutrient application. From the series of uniformly distributed random day combinations, one will be selected and incorporated into the lower-level optimization.Lower-level optimization The agricultural management strategy is optimized by the online data-driven approach proposed in Algorithm 1. Assuming three irrigation and three nitrogen application events are given, these events will be incorporated into the LOP, which consists of the RBF and NSGA-II. The population size of this paper is 105. The number of iterations varies according to the different strategies, and the objective function values are calculated by DSSAT. The main idea of applying Evolutionary multi-objective algorithms(EMO) and RBF to DSSAT is to generate a large number of trial offspring by traditional Simulated Binary Crossover (SBX) and Polynomial Mutation (PM), and then evaluate them using the trained surrogate model50. The objective values of the evaluation were then ranked by Pareto non-dominated and crowding distance, and the top 105 individuals were selected from a large number of trial offspring, after which a small number of individuals out of 105 were selected by Maximum Extension Distance (MED) for real function evaluation, and then combine the parents and offspring to select the next generation of parents by Pareto non-dominated and crowding distance sorting. Furthermore, in the numerical experiments, to ensure the superiority of the algorithm and reduce the experimental complexity, we use a relatively simple radial basis function (RBF) surrogate. The NSGA-II algorithm can be used for both bi-objective and tri-objective problems, so it can optimize the system by starting with the most critical objective and then adding additional objectives. For each solution in the population, the objective functions (1: maximize yield, 2: minimize irrigation application, 3: minimize nitrogen fertilizer application) will be evaluated by invoking the DSSAT model for these dates and the amount of fertilizer irrigation applied. Populations will be tested against the termination criteria (maximum number of iterations allowed). If the termination criteria are not satisfied, the population evolves and is re-evaluated again. The process is repeated until the termination criterion is satisfied and then the local Pareto front of the selected day combination is stored. After each iteration of the UOP, the new local Pareto is combined with the global Pareto frontier. In the next step, if there are any remaining day combinations, the above process is repeated for each new day combination until all generated random day combinations have been processed.Lower-level screening Firstly, the K-means method is used to screen the global Pareto solutions with higher yield. Then, secondary screening takes economic efficiency as the objective and optimizes it by Differential Evolution (DE) algorithm. Finally, the locally appropriate solution is intelligently selected.Optimization strategies and configurationDue to the complexity of the problem, a BSBOP framework was proposed in this study. Due to a large number of variables behind irrigation and fertilization, traversal date for optimization appears to be particularly difficult and time-consuming, assuming that only irrigation is optimized for 120 days of the growth cycle and the decision-maker has 0-150 mm of water per day, then there are ({151}^{120}) different solutions. If both irrigation and fertilization are considered, then there are ({151}^{120}cdot {151}^{120}) different solutions. Therefore, this study tries to reduce the number of variables while minimizing the running time of the algorithm.Here we hypothesize that more precision and effective agricultural management can be implemented through the proposed framework. Not only can crop yields be increased, but also irrigation application and fertilizer application can be reduced, while the solutions obtained have important guidance for decision-makers: such as the selection of irrigation and fertilizer application dates during the growing season of the crop, the selection of irrigation and fertilizer application amounts, and the relationship between economic benefits and application costs. To test this hypothesis, different optimization strategies were developed and evaluated (Table 1). Each optimization strategy was aimed at maximizing yield while minimizing resource wastage.The various strategies are listed below (Table 1). Strategy 1—Fixed irrigation dates: Keeping the number of irrigation days and all parameters constant, only the amount of irrigation on each date is changed, trying to reduce the amount of irrigation as much as possible, make it easy to compare the results with best practices. Strategy 2—Optimal irrigation dates: Traverse through the irrigation dates to optimize irrigation, and try to find a better combination of irrigation dates (optimal dates) and better amount of irrigation over the wheat growth cycle. Strategy 3—Optimal irrigation dates based on surrogate model: RBF is added to Strategy 2, which makes it possible to reduce lots of time. Strategy 4—Fixed fertilizer application date: Using the optimal irrigation date found in Strategy 2 while keeping the number of days of fertilization and all other parameters constant, irrigation and fertilization are optimized in an attempt to minimize the amount of irrigation and fertilizer applied. Strategy 5—Optimal fertilizer application date: while ensuring the optimal irrigation date, traverse the fertilizer application date for optimization, trying to find out the potential yield of the crop. Strategy 6—Optimal fertilizer application date based on surrogate model: RBF is introduced based on Strategy 5. The time consumption was reduced.The stopping criterion in this study is when the optimization results converge visually. The algorithm population size was set to 105, and the generation of offspring used traditional polynomial Mutation. 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Identification of Elovl genes from E. tetradactylum and E. rhadinumTotally, we successfully identified 9 Elovl genes, including elovl1a, elovl1b, elovl4a, elovl4b, elovl5, elovl6, elovl6l, elovl7a, and elovl8b, both from E. tetradactylum and E. rhadinum genome (Table 2). In E. rhadinum, the shortest and the longest putative CDS length among all Elovl genes was 810 bp and 2019 bp, respectively. Their encoded protein size ranged from 269 amino acids to 672 amino acids. The theoretical molecular weight of Elovl proteins varied from 31061.48 to 75051.42 Da, with the theoretical isoelectric points (pI) ranging from 7.86 to 9.59. Most of the Elovl proteins were characterized as stable and hydrophilic proteins. Signal peptide prediction analysis showed that the elovl1b, elovl5, and elovl6 contained signal peptide sequences. In addition to elovl8b, all Elovl proteins contained transmembrane domains ranging from 5 to 7. Almost all Elovl proteins were predicted to be endoplasmic reticulum-located except elovl8b, predominantly localized in the nucleus.Table 2 Basic information for the Elovl gene family members.Full size tableIn E. tetradactylum, the putative CDS length of Elovl genes ranged from 810 to 1824 bp, and their encoded protein size ranged from 269 amino acids to 409 amino acids. The molecular weight of Elovl proteins varied from 31049.42 to 68750.14 Da, with the pI ranging from 8.72 to 9.64. Like Elovl proteins in E. rhadinum, most elovl proteins were predicted to be stable and hydrophilic. Signal peptide prediction analysis revealed that elovl1a, elovl5, and elovl6 had signal peptide sequence, which was different from E. rhadinum that elovl1b contained signal peptide sequence, but elovl1a did not. In addition, seven members showed the same number of transmembrane structures with E. rhadinum, while the elovl8b contained three and elovl4b contained seven transmembrane structures in contrast to E. rhadinum. The elovl8b was predicted to be localized in nuclear, while other members were localized in the endoplasmic reticulum, similar to E. rhadinum.Evolution of divergence and conservation of Elovl genesDivergence and conservation accompany the process of species evolution. To elucidate the phylogenetic relationship of Elovl genes among different species, a maximum like-hood tree was constructed on the basis of 18 Elovl genes in E. tetradactylum and E. rhadinum and 106 publicly available Elovl protein sequences. As shown in Fig. 1, these Elovl genes can be divided into eight subfamilies, including elovl1a/1b, elovl2, elovl3, elovl4a, elovl5, elovl6/6 l, elovl7a/7b, elovl8a/8b. However, 6 subfamilies were presented in the Eleutheronema genus, and there was only one subtype for elovl7 (elovl7a) and elovl8 (elovl8b) in E. tetradactylum and E. rhadinum. The elovl3 was mainly identified in mammalians such as Homo sapiens and Mus musculus, while a recent study reported a full repertoire of Elovl genes in the Colossoma macropomum genome, including elovl330. The loss of elovl2 occurred in the vast majority of marine fish lineages, which was only presented in a few fish species, such as C. carpio, D. rerio, S. salar, and S. grahami.Figure 1Phylogenetic tree for 18 Elovl proteins from E. tetradactylum and E. rhadinum, and 106 publicly available Elovl proteins from other species. All these proteins were aligned using ClustalW and then subjected to MEGAX for phylogenetic tree construction using the maximum like-hood method with 1000 replicates.Full size imageWe further performed the gene structure analysis to visualize the exon–intron structure of each gene, and the results revealed that the elovl8b had the largest intron number, while the elovl6/6 l subfamily genes contained three introns (Fig. 2a). Except for elovl8, Elovl genes belonging to the same subfamily shared a similar gene structure. Additionally, we identified ten motifs in Elovl genes, and the conversed motif types, numbers, and distributions in Elovl proteins were much more similar except for the elovl8b (Fig. 2b, TableS1). Two conserved motifs were found in the Elovl gene family except for elovl8b in E. rhadinum, which were related to the ELO domain via SMART evaluation analysis (Fig. 2c and d). Gene structural variation is important for gene evolution. In E. tetradactylum and E. rhadinum, Elovl genes showed similar gene structure, and the proteins shared similar motif compositions, indicating that the Elovl genes were highly conserved in the Eleutheronema genus.Figure 2Gene structure and conserved motifs diagram of Elovl genes. (a) Gene structure of Elovl genes. Exons were represented by pink boxes and introns by black lines; (b) Conserved motifs of Elovl proteins; (c and d) Logo representations of the ELO domains, motifs 1 and 2, respectively.Full size imageIn the process of evolution via natural selection, adaptation to certain environmental conditions likely drove the changes in endogenous capacity for LC-PUFA biosynthesis between marine and freshwater fishes31. The Elovl gene family has been functionally studied and characterized in a variety of fish species, and the member of the Elovl gene family of each species varied greatly. In the present study, for a comprehensive analysis of Elovl genes in the Eleutheronema genus, the Elovl gene ortholog clusters of mammals and various teleosts with different ecological niches and habitats were collected. The results showed that only seven Elovl genes (one gene for each subtype) were observed in mammals; however, more members were variably presented in teleosts, which might be related to the teleost-specific duplication. A previous study revealed that Sinocyclocheilus graham and C. carpio possessed the highest number of Elovl genes, containing 21 members of subtypes, resulting from an extra independent 4th whole-genome duplication event32, 33. Interestingly, only 9 Elovl genes were observed in Eleutheronema genus, the same as T. rubripes, possibly due to gene loss and the asymmetric acceleration of the evolutionary rate in one of the paralogs following the whole-genome duplication in some teleost fishes34. Additionally, the elovl2 and elovl3 were absent, but a novel subtype, elovl8, was present in most marine fishes. The elovl8, the most recently identified and novel active member of the Elovl protein family member, has been proposed to be a fish-specific elongase with two gene paralogs (elovl8a and elovl8b) described in teleost35. In Eleutheronema, we also found that the elovl8b was presented in E. tetradactylum and E. rhadinum, indicating the important roles in the LC-PUFAs biosynthesis of Eleutheronema fish. Similar results were also observed in rabbitfish and zebrafish20. The Elovl gene family member number in Eleutheronema genus is the same as T. rubripes, but less than I. punctatus (10), Gadus morhua (10), D. rerio (14), S. salar (18), and C. carpio (21), which might be due to the differential expansion events during the evolutions of fish species.Predicting the protein structure is a fundamental prerequisite for understanding the function and possible interactions of a protein. In the present study, the secondary structures as well as three-dimensional structures of Elovl proteins in both E. tetradactylum and E. rhadinum were predicted using the SOPMA and Phyre2 programs, respectively. The protein structures of all the candidate Elovl proteins were modeled at  > 90% confidence. The secondary structures of these proteins in E. tetradactylum revealed 40.86–50.30% alpha helixes, 28.10–28.10% random coil, 13.75–20.67% extended strand and 2.38–4.47% beta turn, while these ratios were predicted to be 47.55–53.27, 30.00–36.01, 6.99–18.12 and 2.38–4.75%, respectively, in E. rhadinum (Table 3). High ratio of alpha helixes and random coil in the Elovl protein structure might play important roles in fatty acids biosynthesis in fish, in accordance with the literature for the order Perciformes in Perca fluviatilis36. Additionally, the secondary structure pattern of Elovl proteins in the candidate E. tetradactylum and E. rhadinum species were highly similar (Fig. 3), indicating the probable similar biological functions as well as highly evolutionarily conserved Elovl genes in Eleutheronema species.Table 3 Properties of the secondary structures of Elovl proteins.Full size tableFigure 3The secondary structure pattern, including alpha helix (blue color), random coil (purple color), extended strand (red color), and beta turn (green color), of Elovl proteins in E. tetradactylum and E. rhadinum.Full size imageThe 3D model results showed that all predicted Elovl proteins had complex 3D structures, composing of multiple secondary structures including alpha-helices, random coils, and others (Fig. 4). The Elovl proteins of different subfamilies showed different 3D configurations. The 3D structures of Elovl proteins also revealed the presence of the conserved domain in each Elovl protein, which showed a typical three-dimensional frame comprising of various parallel alpha-helixes. To assay the quality and accuracy of the predicted 3D model for the candidate Elovl proteins, the Ramachandran plot analysis was employed (Figure S1). In model validation, the qualities of the Elovl proteins model varied from 90 to 98% based on the Ramachandran plot analysis, suggesting the reasonably good quality and reliability of the predicted 3D models. These results indicated that the predicted 3D model of Elovl proteins could provide valuable information for the further comprehensive studies of molecular function in the fatty acids biosynthesis in Eleutheronema species. Additionally, the comparisons between these structures in E. tetradactylum and E. rhadinum suggested that the Elovl proteins encompassed the conserved structures. In addition, gene duplication resulted in obvious 3D structural variation in the duplicated genes, such as Elovl4 (elovl4a and elovl4b), Elovl6 (elovl6 and elovl6l). The ascertained variations were revealed in duplicated Elovl proteins, and the diversities in these proteins structure may reflect their different obligations in the fatty acid biosynthesis and other biological processes.Figure 4Three-dimensional modeling of Elovl proteins in E. tetradactylum and E. rhadinum. All models have confidence levels above 90%.Full size imageTo explore the functional selection pressures acting on Elovl gene family, Ka, Ks, and Ka/Ks ratios were calculated for each gene. Generally, Ka/Ks  1 indicates positive selection. In this study, we found that all the Ka/Ks ratios for each gene were less than 0.5, suggesting that they were subjected to strong purifying selection during evolution, and their functions might be evolutionarily conserved (Fig. 5). Therefore, theoretically, the Elovl genes in the Eleutheronema genus had eliminated deleterious mutations in the population through purification selection. Similar results were also observed in Elovl gene family of Gymnocypris przewalskii that no positive selection trace was detected in most members except elovl211. Moreover, elovl6l and elovl8b showed a higher average Ka/Ks ratio than the other seven members, indicating that the evolution of elovl6l and elovl8b might be much less conservative and thereby could provide more variants for natural selection in Eleutheronema species.Figure 5The evolutionary rates of the Elovl genes in (a) E. tetradactylum and (b) E. rhadinum. The Ka, Ks, and Ka/Ks values were demonstrated in boxplots with error lines.Full size imageChromosomal location, collinearity, and protein–protein interaction network analysis of Elovl genesAs shown in Fig. 6a and b, Elovl genes were randomly and unevenly distributed on seven chromosomes in both E. tetradactylum and E. rhadinum, including Chr5, Chr6, Chr8, Chr10, Chr11, Chr13, and Chr25. The Chr5 and Chr6 harbored two Elovl genes (elovl1b and elovl8b in Chr5, elovl5 and elovl6l in Chr6), while other chromosomes each carried a single Elovl gene. Collinearity relationship analysis was performed to further investigate the gene duplication events within the Elovl gene family. The results revealed that a pair of segmental duplication genes (elovl4a/4b) showed collinear relationships. A chromosome-wide collinearity analysis also showed that the chromosomes were highly homologous between E. tetradactylum and E. rhadinum, including the Elovl gene family (Figure S2). To infer the protein interaction within Elovl gene family, we constructed the protein–protein interaction (PPI) network of the Elovl proteins based on the interaction relationship of the homologous Elovl proteins in zebrafish. The results showed that Elovl genes had close interaction with other members except for the elovl4a/4b and elovl8b (Fig. 6c), which suggested that they might participate in diverse functions by interacting with other proteins. Thus far, elovl4a and elovl4b were widely identified in most fish, which could effectively elongate PUFA substrates37. In addition, the elovl4a/4b were identified to be homologous proteins of zebrafish, indicating that the elovl4 subtype was highly conserved during evolution and played important roles in the biosynthesis of LC-PUFA in Eleutheronema.Figure 6Chromosomal location and collinearity analysis of Elovl gene family in (a) E. tetradactylum and (b) E. rhadinum. Colored boxes represented chromosomes. Segmental duplication genes are connected with grey lines; (c) a protein–protein interaction network for Elovl genes based on their orthologs in zebrafish.Full size imageExpression patterns of ELOVL genes in different tissuesIn the present study, we aimed to determine the expression patterns and gained insights into the potential functions of Elovl genes in the brain, eye, gill, heart, kidney, liver, muscle, stomach, and intestine. The expression patterns of Elovl genes in different tissues and species were distinct, suggesting the diverse roles during fish development (Fig. 7a and b). In our present study, the elovl1a and elvovl1b were expressed in a relatively narrow range of tissues, including the liver, stomach, and intestine. Some Elovl genes had much higher relative expression rates, e.g., elovl1a and elovl7a. The elovl4a was primarily distributed in the brain and eye, slightly expressed in gills while hardly detectable in other tissues, consistent with previous studies37, 38, which might play an important role in endogenous biosynthesis of LC-PUFA in the neural system of fish. In contrast to elovl4a, elovl4b was ubiquitously, instead of tissue-specific, expressed in most tissues while hardly examined in the heart and kidney. The elovl4a and elovl4b were two commonly paralogues in evolutionarily diverged fish species, and the striking difference in expression patterns between elovl4a and elovl4b might be due to the potential functional divergence of these two paralogues. In addition, elovl8b, the novel active member of the Elovl protein family, was expressed in several tissues, suggesting the essential roles in LC-PUFAs biosynthesis of teleost as indicated by a previous study20. Moreover, the differences in expression patterns among different Elovl genes indicated that these genes might possibly undergo functional divergence during evolution in the Eleutheronema genus. Overall, our present study firstly provided the preliminary organ-specific expression data of the Elovl gene family in E. tetradactylum and E. rhadinum, which could provide the foundation for further clarifying the function of these genes in the evolutionary development of the Eleutheronema genus.Figure 7qPCR assessment of tissue distribution of elovl1a, elovl1b, elovl4a, elovl4b, elovl5, elovl6, elovl6l, elovl7a, and elovl8b gene expression in (a) E. tetradactylum and (b) E. rhadinum for various tissues including the brain, eye, gill, heart, kidney, liver, muscle, stomach, and intestine.Full size image More

Study site descriptionThe study was carried out at the edge of an arid region in mature plantations dominated by P. halepensis, of age of 40-50 years (Pinus halepensis), and their adjacent non-forested ecosystems. The sites were distributed across a climatic gradient from arid and semi-arid to dry sub-humid (Fig. 1, Supplementary Table S1). Three selected paired sites included: (1) An arid site at Yatir forest (annual precipitation, P: 280 mm; aridity index, AI: 0.18; elevation: 650 m; light brown Rendzina soil, and forest density: 300 trees ha−1), where a permanent flux tower has been operating since the year 2000 (http://fluxnet.ornl.gov). Note that an AI of 0.2 marks the boundary between arid and semi-arid regions. Yatir, with AI = 0.18, is formally within an arid zone, but on the edge of a semi-arid zone. (2) An intermediate semi-arid site in Eshtaol forest (P: 480 mm; AI: 0.37; elevation: 350 m; light brown Rendzina soil, and forest density: 450 trees ha−1). (3) A dry-subhumid site in northern Israel at the Birya forest (P: 770 mm; AI: 0.64; elevation: 755 m; dark brown Terra-Rossa and Rendzina soil, and forest density: 600 trees ha−1). Non-forest ecosystems were sparse dwarf shrublands, dominated by Sarcopoterium spinosum in a patchy distribution with a wide variety of herbaceous species, mostly annuals, that grew in between the shrubs during winter to early spring, and then dried out. All non-forested sites had been subjected to livestock grazing (exposing soils). Finally, an additional site that was characterized as Oak-forest vegetation was added. The site was dominated by two oak species, Quercus calliprinos and Quercus ithaburensis (P: 540 mm; AI: 0.4; see previous publication for more details on the oak site53). All sites were under high solar radiation load, with an annual average of approximately 240 Wm−2 in the arid region and only 3% lower in the northern site in the dry-subhumid region (Table 1).Mobile laboratoryMeasurements were conducted on a campaign basis using a mobile lab with a flux measurement system at all sites except the Yatir forest, where the permanent flux tower was used (http://fluxnet.ornl.gov;54). Repeated campaigns of approximately two weeks at each site, along the seasonal cycle, were undertaken during 4 years of measurements, 2012–2015 (a total of 6-7 campaigns per site, evenly distributed between the seasons) the 4 years of measurements were found to be representative of previous 70 years of precipitation record (Supplementary Figure S1 and Table S2). The mobile lab was housed on a 12-ton 4 × 4 truck with a pneumatic mast with an eddy-covariance system and provided the facility for any auxiliary and related measurements. Non-radiative flux measurements were undertaken using an eddy-covariance system to quantify CO2, sensible heat (H), and latent heat (LE) fluxes using a 3D sonic anemometer (R3, Gill Instruments, Hampshire, UK) and an enclosed-path CO2/H2O infrared gas analyzer (IRGA; LI-7200, LI-COR). Non-radiative flux measurements were accompanied by meteorological sensors, including air temperature (Ta), relative humidity (RH), and pressure (Campbell Scientific Inc., Logan, UT, USA), radiation fluxes of net solar- and net long-wave radiation (SWnet and LWnet, respectively), and photosynthetic radiation sensors (Kipp & Zonen, Delft, Holland). Raw EC data and the data from the meteorological sensors were collected using a computer and a CR3000 logger (Campbell Sci., Logan, UT, USA), respectively. The EC system was positioned at the center of each field site with the location and height aimed at providing sufficient ‘fetch’ of relatively homogeneous terrains. For detailed information on the use of the mobile lab and the following data processing of short and long-term fluxes see previous publications29,55,56.Data processingMean 30-min fluxes (CO2, LE, and H) were computed using Eddy-pro 5.1.1 software (LiCor, Lincoln, Nebraska, USA). Quality control of the data included a spike removal procedure. A linear fit was used for filling short gaps (below three hours) of missing values due to technical failure. Information about background meteorological parameters, including P, Ta, RH, and global radiation (Rg), was collected from meteorological stations (standard met stations maintained by the Israel Meteorological Service, https://ims.gov.il/en). The data were obtained at half-hourly time resolution and for a continuous period of 15 years since 2000.Estimating continuous fluxes using the flux meteorological algorithmEstimation of the flux-based annual carbon and radiation budgets was undertaken using the short campaign measurements as a basis to produce a continuous, seasonal, annual, and inter-annual scale dataset of ecosystem fluxes (flux meteorological algorithm). The flux meteorological algorithm method was undertaken based on the relationships between measured fluxes (CO2, LE, H, SWnet, and LWnet) and meteorological parameters (Ta, RH, Rg, VPD, and transpiration deficit, a parameter that correlated well with soil moisture, see main text and supplementary material of previous publication29. A two-step multiple stepwise regression was established, first between the measured fluxes (H, LE, and the ecosystem net carbon exchange) and the meteorological parameters measured by the mobile lab devices, and then between the two meteorological datasets (i.e., the variables measured by the Israel meteorological stations) for the same measurement times. Annual fluxes were calculated for the combined dataset of all campaigns at each site using the following generic linear equation:$$y={{{{{rm{a}}}}}}+{Sigma }_{i}{b}_{i}{x}_{i}$$
(1)
where, y is the ecosystem flux of interest, the daily average for radiative fluxes (LWnet and SWnet), non-radiative fluxes (H and LE), and daily sum for net ecosystem exchange (NEE), a and ({b}_{i}) are parameters, and ({x}_{i}) is Ta, RH, Rg, vapor pressure deficit, or transpiration deficit. The meteorological variables (({x}_{i})) were selected by stepwise regression, with ({b}_{i}=0) when a specific ({x}_{i}) was excluded.Based on this methodology, ecosystem flux data were extrapolated to the previous 7–15 years (since 2000 in the dry-subhumid and arid sites, since 2004 in the semi-arid sites, and since 2008 in the Oak-forest site) using all the available continuous meteorological parameters from the meteorological stations associated with our field sites. The long-term annual sums and means of extrapolated ecosystem fluxes were averaged for multi-year means of each site for the period of available extrapolated data. In the first, previously published phase of this study29, the extrapolation method was extensively tested, including simulation experiments at the arid forest site, where continuous flux data from the 20 years old permanent flux tower were available. Five percent of the daily data were selected by bootstrap (with 20 repetitions), a stepwise regression was performed for this sample, and then, the prediction of fluxes using Eq. 1 above was performed for the entire observation period. In the current phase of the study additional flux measurements are included with the R2 coefficients for the additional measurements ranging between 0.4-0.9, see Supplementary Table S3.The aridity index of the Oak-forest was in between those of the semi-arid and dry-subhumid Pine-forests (0.4 compared to 0.37 and 0.67, respectively). Therefore, to compare the Oak-forest with Pine-forest and non-forest sites, the average results from the semi-arid and dry-subhumid paired sites were used.Radiative forcing and carbon equivalence equationsTo compare the changes in the carbon and radiation budgets caused by forestation, we adopted the approach of Myhre et al. 30, and used Eq. 2:$${{RF}}_{triangle C}=5.35{{{{mathrm{ln}}}}}left(1+frac{triangle C}{{C}_{0}}right),left[W,{m}^{-2}right]$$
(2)
where land-use changes in radiative forcing (RFΔC) are calculated based on the CO2 reference concentration, C0 (400 ppm for the measured period of study), and ΔC, which is the change in atmospheric CO2 in ppm, with a constant radiative efficiency (RE) value of 5.35. Here, ΔC is calculated based on the annual net ecosystem productivity (NEP; positive carbon gain by the forest, which is identical to net ecosystem exchange (NEE), the negative carbon removal from the atmosphere) as the difference between forested and non-forested ecosystems (ΔNEP) multiplied by a unit conversion constant:$$triangle C={left[{overline{{NEP}}}_{F}-{overline{{NEP}}}_{{NF}}right]}_{[gC{m}^{-2}{y}^{-1}]}cdot k ,[{ppm}]$$
(3)
where, k is a unit conversion factor, from ppm to g C (k = 2.13 × 109), calculated as the ratio between the air molar mass (Ma = 28.95; g mol−1), to carbon molar mass (Mc = 12.0107; g mol−1), and total air mass (ma = 5.15 × 109; g).Etminan et al. 57 introduced an updated approach to calculate the RE as a co-dependent of the change in CO2 concentration and atmospheric N2O:$${RE}={a}_{1}{left(triangle Cright)}^{2}+{b}_{1}left|triangle Cright|+{c}_{1}bar{N}+5.36,left[W,{m}^{-2}right]$$
(4)
where, (triangle {{{{{rm{C}}}}}}) is the change in atmospheric CO2 in ppm resulting from the forestation, as calculated in Eq. 3, (bar{{{{{{rm{N}}}}}}}) is the atmospheric N2O concentration in ppb (323), and the coefficients a1, b1, and c1 are −2.4 × 10−7 Wm−2ppm−1, 7.2 × 10−4 Wm−2 ppm−1, and −2.1 × 10−4 Wm−2ppb−1, respectively.Combining Eqs. 2 and 4 with an airborne fraction of (zeta =0.44)58, we obtain Eq. 5:$${{RF}}_{triangle C}={RE}cdot {{{{mathrm{ln}}}}}left(1+frac{zeta cdot triangle C}{{C}_{0}}right),left[W,{m}^{-2}right]$$
(5)
Next, the annual average radiative forcing due to differences in radiation flux was calculated as follows:$${{RF}}_{triangle R}=frac{triangle Rcdot {A}_{F}}{{A}_{E}},left[W,{m}^{-2}right]$$
(6)
where, ΔR is the difference between forest and non-forest reflected short-wave or emitted long-wave radiation (ΔSWnet and ΔLWnet, respectively), assuming that the atmospheric incoming solar and thermal radiation fluxes are identical for the two, normalized by the ratio of the forest area (({A}_{F})) to the Earth’s area (({A}_{E}=5.1times {10}^{14},{m}^{2})).As forest conversion mostly has a lower albedo, the number of years needed to balance (‘Break even time’) the warming effect of changes in radiation budget by the cooling effect of carbon sequestration is calculated by combining Eqs. 5 and 6:$$^prime{Break},{even},{time}^prime=frac{{{RF}}_{triangle alpha }}{{{RF}}_{triangle C}},[{{{{{rm{years}}}}}}]$$
(7)
The multiyear averages of NEP for each of the three paired sites (forest and non-forest) were then modeled over a forest life span of 80 years. This was done based on a logarithmic model, modified for dryland, which takes as an input the long-term averages of NEP ((overline{{NEP}})) as in Eq. 3:$${{NEP}}_{t}=overline{{NEP}}(1-{exp }^{bcdot t}),left[g{{{{{rm{C}}}}}},{{{{{{rm{m}}}}}}}^{-2}{{yr}}^{-1}right]$$
(8)
where annual carbon gain at time t (NEPt) is a function of the multiyear average carbon gain ((overline{{{{{{rm{NEP}}}}}}})), forest age (t), and growth rate (b). Parameter b is a constant (b = −0.17) and is calculated based on the global analysis of Besnard et al. 59, limiting the data to only dryland flux sites60. Note that this analysis indicates NEP reaching a steady state and was used here to describe the initial forest growth phase, while growth analyses indicate that carbon sequestration peaks after about 80 years, followed by a steep decline50. This is consistent with the time scale for forest carbon sequestration considered here.In contrast to the one-year differences presented in Table 1 (ΔNEP), the net sequestration potential ((triangle)SP) for each of the paired sites was calculated as the accumulated ecosystem ΔNEPt along with forest age ((triangle) is the difference between forest and non-forest sites):$$triangle {SP}=mathop{sum }limits_{t=0}^{{age}}{triangle {NEP}}_{t}/100,left[{{{{{rm{tC}}}}}},{{{{{{rm{ha}}}}}}}^{-1}{{age}}^{-1}right]$$
(9)
The ΔSP growth model was compared with previously published data of long-term carbon stock changes in arid forests (i.e., cumulative NEP over 50 years since forest establishment, t = 50), demonstrating agreement within ± 10%27.For comparison with previous studies, the carbon emission equivalent of shortwave forcing (EESF) was calculated using an inverse version of Eqs. 5 and 6 based on Betts1:$${EESF}={C}_{0}left({e}^{frac{{{RF}}_{triangle R}}{zeta cdot {RE}}}-1right)cdot k/100,left[{{{{{rm{tC}}}}}},{{{{{{rm{ha}}}}}}}^{-1}{{age}}^{-1}right]$$
(10)
where, C0 is the reference atmospheric CO2 concentration (400 ppm, the average atmospheric concentration for the past decade), RFΔR is the multiyear average change in radiative forcing as a result of the change in surface albedo (Eq. 6 W m−2), RE is the radiative efficiency (Eq. 4, W m−2), ζ is the airborne fraction (0.44 as in Eq. 5), and k is a conversion factor, from ppm to g C (2.13 × 109 as in Eq. 3). Equation 10 was also used to calculate the emission equivalent of longwave forcing (EELF) with the RFΔR as the multiyear average change in radiative forcing as a result of the change in net long-wave radiation (ΔLWnet).Finally, the net equivalent change in carbon stock due to both the cooling effect of carbon sequestration and the warming effect due to albedo change (net equivalent stock change; NESC), was calculated by a simple subtraction:$${NESC}=triangle {SP}-{EESF},left[{{{{{rm{tC}}}}}},{{{{{{rm{ha}}}}}}}^{-1}{{age}}^{-1}right]$$
(11)
A comparison of the ΔSP (Eq. 9), the EESF (Eq. 10), and NESC (Eq. 11) with the same metrics as those used in other studies1,14,61 was done when appropriate. An exception was made for Arora & Montenegro (2011), where only carbon stock changes (ΔSP) were available in carbon units, and biogeophysical (BGP) and biogeochemical (BGC) effects were expressed as temperature changes. To overcome this metric difference, we converted the biogeophysical to carbon equivalent units (EESF + EELF) by multiplying the carbon stock changes (ΔSP) by the ratio between the BGP and BGC effects on temperature (EESF + EELF = ΔSP × BGP/BGC).Statistical and data analysesThe paired t-test was used to compare multi-annual averages of all variables between forested and adjacent non-forested sites and between sites across the climatic gradient. The variables of interest that were detected for their significant differences were albedo, net radiation and its longwave and shortwave components, latent heat fluxes, sensible heat fluxes, and net ecosystem productivity. All statistical and data analyses were performed using R 3.6.0 (R Core Team, 2020)62.Reporting summaryFurther information on research design is available in the Nature Portfolio Reporting Summary linked to this article. More

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